Introduction

Rapidly emerging novel treatments in oncology, particularly in advanced disease, mean that more patients are living longer [1]; for those who cannot be cured, the goal of therapy is extending survival whilst maintaining or improving quality of life. This changing landscape has implications for the tools both researchers and clinicians have at their disposal to evaluate and improve patient outcomes holistically.

The measurement of a patient’s subjective experience of both the symptoms of disease and treatment-related toxicity within clinical trials has increased [2, 3]. This practice is expanding to routine care and follow-up [4, 5] with the concept of health-related quality of life (HRQoL) subsumed under the broader term of patient-reported outcomes (PROs). Good, well-validated HRQoL instruments have been used in oncology for some time, measuring the impact of disease on functioning and well-being. Many checklists and subscales are available enabling measurement of treatment related side effects as well as symptoms of disease. These are usually designed for use with more generic HRQoL questionnaires revealing the overall impact that disease and treatment may exert on physical, functional, emotional and social well-being. The best validated, generic patient-reported outcome measures (PROMs) used most frequently are the European Organisation for Research and Treatment of Cancer (EORTC) QLQ-C30 [6] and the Functional Assessment of Cancer Therapy (FACT-G) [7] questionnaires. Both have disease-specific cancer modules or subscales, but the FACT has a wider range of treatment-specific subscales.

Although the more frequent use of PROMs is encouraging, there may well be areas of concern impacting the quality of survival that are insufficiently assessed. A previous systematic review by Muzzati and Annunziata [8] showed that some PROMs examine different and limited aspects of patients’ social well-being. For example the subscale of the EORTC QLQ-C30 refers to social and role functioning, the FACT-G to relatives and relationships and the Psychological Screen for Cancer [9] to social support. The authors of this previous systematic review [8] commented that none of the multidimensional HRQoL instruments totally captured the complexity of ‘social impact’. This led them to a systematic search of instruments dedicated solely to the assessment of the social aspects of the cancer experience (or validated in cancer populations) which yielded 27 articles relating to 14 instruments. The social dimensions covered by these tools were predominantly communication (couple/family/caregiver), relationships (with family and friends) and support (from family and friends) and are a reflection of the search terms derived from the social items listed in existing HRQoL measures and a limiting factor of the review. By deriving the search terms using this method, it is not surprising to have identified tools that measure similar issues to those of the social domains of the HRQoL instruments, but potentially covering them in greater depth. Our contention is that the literature on the social concerns and issues faced by cancer patients contains a broader spectrum of social issues than the items on those existing HRQoL instruments. Though Muzzati and Annunziata’s review systematically searched for more depth, it failed to extend its range potentially missing areas of interest. The review did identify one instrument, the Social Difficulties Inventory [10], which included an ‘everyday living’ subscale examining care of dependents, recreation and independence and a ‘money matters’ subscale with items on work, finances and welfare benefits. The social problems that patients with cancer have has been documented for some considerable time with early literature showing that problems can be experienced with employment [11–13], managing daily living [12, 14], finances [15, 16] and insurance [13, 17]. Later work has continued to reveal the social issues that cause significant concern for patients. Both qualitative research [18–20] and pure economic surveys/evaluations [21–25] illustrate that financial worry and hardship are both evident and prevalent. Furthermore, quantitative reports of return to work rates and functional abilities in terms of work performance and obstacles [26–33] and qualitative studies exploring the importance and meaning of work for patients [34, 35] serve to underline the salience of this area. Qualitative studies demonstrate that roles and responsibilities outside of work (i.e. being a parent or carer for others) are also a significant part of patients’ lives and that cancer has consequent interaction and impact on these [36–40]. Wright and colleagues [41] conducted a robust study with patients using focus groups and interviews to describe and categorise cancer patients’ social difficulties. A total of 32 social problems were identified which were able to be categorised under eight headings: (1) managing in the home, (2) health and welfare services, (3) finances, (4) employment, (5) legal matters, (6) relationships, (7) sexuality and body image and (8) recreation. This literature suggests a breadth of social aspects of patients’ lives impacted by cancer that is not traditionally captured alongside treatment toxicity and disease burden, endorsing the need for a further literature search focussed on PROs covering the areas not so well accounted for by the commonly used HRQoL measures.

The current review aims to provide summary and evaluation of PROMs used in studies for reporting the impact of cancer on wider social aspects of patients’ lives, particularly those which may be salient to living with the illness for an extended period, in other words, expanding assessments to look at lifestyle impacts under a conceptual framework which is in the early stages of delineation and referred to as ‘quality of survival’ (defined by four interconnected dimensions: survival, quality of life, side effect management and economic impact management) [42]. This will highlight what has been used, and how and where gaps may still exist which could be addressed with revision or supplementation of currently employed tools. The focus is on the patient with cancer, not caregivers nor relatives (see Shilling et al. [43] for a review of caregiver impact measures).

Methods

Data sources and search

We followed the general principles published by the NHS Centre for Reviews and Dissemination [44] and carried out an electronic search of databases to identify publications using PROs to evaluate the impact of cancer on social aspects of patients’ lives, specifically financial, lifestyle and occupational circumstances, along with roles and responsibilities with dependents (looking after young offspring, a spouse or elderly parents).

Searches were run in MEDLINE (MEDLINE(R) in-process and other non-indexed citations and MEDLINE(R) 1946-present) and EMBASE (1947-present) (both via OvidSP) and CINAHL (1937-present) and PsycINFO (from 1800s–present) (both via EBSCOhost). Terms were modified as appropriate for each database and limited to English language only. A combination of controlled syntax (MeSH) and free-text terms were used. Two groups of terms were generated describing (i) the population and (ii) social aspects of interest. The terms within each group were combined with a Boolean OR command and were searched in combination using a Boolean AND command. Searches were run on 5 March 2015 and an update conducted 8 January 2016 (see Box 1 for the search strategy used for MEDLINE, adapted for other databases). The reference lists of pertinent review articles were also checked for relevant articles.

Box 1: Search strategy used in MEDLINE and adjusted for other databases

1. exp neoplasm/

2. (neoplasm* or cancer).mp.

3. 1 or 2

4. (‘role burden*’ or ‘impact on leisure’ or ‘impact on lifestyle’ or ‘impact on life style’ or ‘role responsibilit*’ or ‘carer responsibilit*’ or ‘childcare role’ or ‘childcare responsibilit*’ or ‘childcare burden*’ or ‘impact on social life’ or ‘social impact’ or ‘family function’).mp.

5. exp return to work/

6. (‘return to work’ or ‘impact on occupation’).mp.

7. 5 or 6

8. (‘out of pocket’ or ‘out-of-pocket’ or ‘financ* burden*’ or ‘financ* impact’ or ‘impact on financ*’).mp.

9. 4 or 7 or 8

10. 3 and 9

11. limit 10 to english language

Study selection criteria

Inclusion criteria were articles in the English language on any quantitative study containing the report of the impact of advanced (or secondary or metastatic or stages III or IV) cancer, as assessed by the use of PROs, on the wider social aspects of adult patients’ lives, that is on financial situation, lifestyle, occupational circumstances, roles and responsibilities with dependents (looking after young offspring or elderly parents) and there was no date restriction.

Excluded were qualitative studies, those with children or caregivers as the sole participants, those involving populations with early cancer (i.e. disease stages I or II) or the very final end-of-life stage; also excluded were studies focussed on the metrics of an instrument, reviews, editorials, letters, opinion, reports published on meeting abstracts and academic theses, any of which an English language version of the PRO had not been developed. Pure monetary costing surveys and functional workability assessment surveys were not included as these give no information on perceived impact on the patient, e.g. recording in a diary a certain amount of money was spent on a hospital parking charge does not establish if, or how, burdensome it was.

A schema for identification and selection of eligible articles can be seen in Fig. 1. Titles and abstracts were screened independently by two reviewers (SC and VS) against the inclusion and exclusion criteria, and any duplicate papers were recorded and excluded. The full text of potentially relevant papers were retrieved and then further scrutinised independently by both reviewers to identify the final list included in the review. Article selection disagreements were resolved by discussion and a third reviewer (LF) provided adjudication if necessary.

Fig. 1
figure 1

Flow chart showing identification and selection of eligible articles

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Citation chasing

Backwards citation chasing (one generation) using reference lists of all papers included in the review and forwards citation chasing (one generation) using Science Citation Index Expanded and Social Science Citation Index Expanded via Web of Science were conducted.

Data extraction

For each included paper, the following descriptive data were extracted into a standardised form: first author name, publication year, setting/country, study design and aim, study population (cancer type and demography), number of participants, what social factor/s were assessed and how, reported outcomes and study limitations. Data were extracted and the quality of studies appraised by one reviewer (RS) and checked by a second (SC or VS). Quality appraisal criteria are shown in Box 2 and were developed in accordance with the principles published by the National Health Service Centre for Reviews and Dissemination [44]. Without evidence to inform any differential weighting amongst the criteria, none was applied. A score of one point was awarded where good evidence was provided to meet a criterion, a half point if the evidence provided was weak, and where no evidence was present a zero score was given. Higher total scores represent better quality with articles scoring 0–3.5 designated a +, scores 4–7.5 a ++ and 8–12 a +++.

Box 2: Criteria for assessing the quality of studies

1. Is the aim of the study clear?

2. Is the study design/method appropriate?

3. Are the study eligibility criteria specified?

4. Is participant selection apparently bias free?

5. Is there a power calculation for sample size?

6. Is sample size adequate and response rate satisfactory? (a possible half point could be given for each)

7. Has a validated measure been used? (i.e. evidence of instrument development, content and construct validity, test-retest reliability, ability to detect change)

8. Are data analyses appropriate?

9. Are all study participants accounted for?

10. Is the study apparently free of confounding factors?

11. Are the conclusions supported by the results?

12. Are the results generalizable?

Results

Articles

The initial search yielded 3115 articles; an additional 6 were identified from hand searches (Fig. 1). After removal of duplicates and initial screening of titles and abstracts, 45 full texts were examined; 12 met the inclusion criteria. A further 8 articles added from the citation searches and 2 from the electronic search update resulted in 22 articles included in the review. The characteristics of the studies are summarised in Table 1, grouped under three broad subheadings dependent upon the focus of investigation: financial distress, roles and responsibilities or multiple aspects of social life. Description of the instruments used and study outcomes is summarised in Table 2.

Table 1 Study characteristics and quality
Full size table
Table 2 Instruments and study outcomes
Full size table

Most articles comprised single time-point surveys covering a broad array of tumour sites. The majority examined mixed tumour groups, but 7/22 reported on single disease groups. Sample size varied widely, ranging from 26 to over 21,000 patients. Overall, sex representation was clearly specified for all of the studies, but details of participants’ ages were less consistently provided. Most of the studies had been conducted within a time frame of the first 3 years following diagnosis. Some study samples were early disease, some clearly advanced disease and others a mixture or details were not provided within the article; however, no specification of stage was made in the inclusion criteria for the current review.

Quality of publications

Marked against the quality criteria in Box 2, and reported in Table 1, only four studies scored highly (+++) [47, 57, 65, 66]. Some individual criteria warrant specific comment. Only 8 studies were rated as having bias free participant selection, 8 were rated as being apparently free of confounding factors and 11 accounted for all participants in their reporting. Of particular note was the use of diverse, non-validated, study-specific instruments to investigate financial distress; only two of 10 studies used a validated measure.

Financial distress

Table 2 details the 10 articles [45–54] that reported on self-perceived financial distress. Only two used a validated measure. One [47] employed ‘The COST measure’ [68], a recently developed 11-item tool validated in patients with advanced cancer and available via the Functional Assessment of Chronic Illness Therapy (FACIT) suite of questionnaires (see www.facit.org). The second [48] used the ‘Personal Financial Wellness (PFW) Scale’ [69] (formally known as the ‘Incharge Financial Distress/Financial Well-Being Scale’ [70]), which has 8 items, is validated and has been used with cancer patients but without normative data [71]. The remaining eight studies [45, 46, 49–54] used un-validated study-specific tools. The number of questions used in these non-validated measures varied widely, and the content of the items across the measures was diverse and highly individual. Outcomes from the 10 articles show the presence of much self-perceived financial distress amongst the study participants. The findings also demonstrated strategies frequently employed by patients to mitigate their financial burden, including financial reductions to health-related areas and more generally with clothing, food and leisure. Additionally, patients borrowed money, used credit and defaulted on bills. Factors repeatedly associated with greater financial burden were younger age, lower income, poorer health status, more treatment/s, non-white ethnicity and poorer psychological well-being (i.e. greater anxiety and depression).

Roles and responsibilities

Three articles [55–57] investigated the impact on patients’ roles and responsibilities in everyday life. Two [55, 56] used the ‘Parenting Concerns Questionnaire’ (PCQ) [72]. Park and colleagues [56] found that patients had mild to moderate concerns about their cancer affecting their parental role, this was both in terms of performing the usual practical things parents do for their children, but was also about the emotional consequences for the child. Of particular concern was how the child would cope with their death, impact of cancer on the child’s emotions and impact on the co-parent’s emotions. Factors associated with higher levels of concerns about parenting were single marital status, poor functional status, poorer quality of life, psychological distress (anxiety and depression) and lack of social support.

Moore et al. [55] combined the use of the PCQ with another tool, the ‘Parental Efficacy Beliefs Scale’, a non-validated instrument measuring patients’ perceptions of their own ability, and that of their co-parent to perform the parental role. Most (60%) felt they had been extremely well able to perform their parenting responsibilities before diagnosis, dropping to 11% after. Similarly, patients reported less belief in the co-parent after diagnosis (42% dropping to 26%). Factors associated with reported decline in parental efficacy were more frequent clinic visits, poorer quality of life and depression. Higher levels of parenting concerns expressed on the PCQ were accompanied by decline in patients’ belief about themselves and their co-parent being able to parent.

Walsh et al. [57] investigated the impact for women with breast cancer on their roles as wife and mother using the ‘Marital’ and ‘Relationship with Children’ subscales from the CARES instrument [73]. Talking to their spouse/partner about what may happen after their death was problematic for 52.8% of the women, and 37.4% indicated that just talking about cancer with them was difficult. Levels of reported difficulty on the Relationship with Children subscale were not high; however, 19.7% reported problems helping their children talk about their cancer, 16.8% helping their children cope and 12.7% taking care of their children as a result of breast cancer.

Multiple aspects of social life

Nine articles used multidimensional instruments [58–66, N.B. 59 and 60 used the same data set]. Five [58–60, 62, 64] utilised the illness intrusiveness rating scale (IIRS) [74], a validated tool which measures the extent to which an illness and/or treatment affects the patient’s social life. Greater levels of intrusiveness were found to be associated with advanced disease, younger age, lower income, cancer type, recent treatment and poor psychological well-being (depression and hopelessness). Conversely, being older, not having children under 18 years living at home, having early stage disease, fewer symptoms and better psychosocial well-being were all associated with consistently low levels of illness intrusiveness. [64].

The finding that cancer and its treatments commonly impact the social aspects of patients’ lives was evident in three papers [63, 65, 66] that had used the Social Difficulties Inventory (SDI), a validated and psychometrically tested instrument [10, 75–78]. In one article with pooled data from three studies, 45% of participants reported high levels of social difficulty, which was associated more with younger age, those with advanced disease and, to some extent, those from deprived areas [65]. In another study, greater social difficulties were found to be associated with invasive disease (lymph node involvement or distant metastases), undergoing surgery, receiving chemotherapy and lower socioeconomic status, and a reduction in difficulties occurred by 10 months follow-up with the apparent disparity between low and high socioeconomic status groups disappearing [63]. Results from nearly 18,000 patients endorsed previous reports that predictors of social difficulties include younger age, living in a more deprived area, having advanced disease and undergoing surgery or chemotherapy [66]. This study also found additional predictive factors were tumour site, non-white ethnicity, receipt of radiotherapy and being a caregiver. The strongest predictor for social distress was found to be having ≥3 long-term co-morbidities, followed by unemployment and recurrent or non-treatable disease.

Social and financial impacts were also reported using a non-validated questionnaire in a study contrasting rural and urban cancer patients’ experiences [61]. Sixty-four percent of patients experienced at least one financial or social consequence, most frequently this was time-off work (44%), reduced income (31%) and missing family events (23%). City dwellers reported significantly more financial impact, but no similar difference was evident for social impact. Those who were younger, currently working and suffering stress, were found to be at higher risk of experiencing financial or social impacts.

Discussion

Though the studies reviewed here were diverse in terms of study objectives, methods and patient populations, the patient-reported outcomes reported by them repeatedly show cancer and its treatments have significant impact on patients’ finances, roles and responsibilities and on the various facets of their social life.

Moreover, the findings complement reports from published quantitative studies [26–33] that have asked patients to report impact objectively (e.g. by reporting how much money they have spent on an item such as a medication, by indicating the time point of return to work or by indicating ability to perform work tasks) and qualitative studies [34–40] providing first-hand patient accounts of burden. All of this together underlines the far broader nature of the aspects of patients’ social lives that are impacted than can be assessed by relying solely on a social function subscale from one of the validated HRQoL instruments frequently in use, e.g. EORCT-QLQ-C30 [6] or FACT-G [7].

The studies reviewed which have attempted to quantify patients’ self-perceived financial distress have all done so using different, and in the majority of cases [45, 46, 49–54], study-specific measures. This has led to diverse and highly individualised content all scored with incomparable rating scales. This makes summarising findings across studies problematic. However, interest and concern regarding financial burden for patients with cancer have been growing recently [24], driven by the rapid pace of change where expensive novel drugs and living longer with incurable disease are now integral to the picture. In response to this pressure, at least one validated PRO, the COST measure [68], has been developed. To improve the quality of studies conducted and data collected in the future, validated instruments such as this need to be consistently and widely used. This may help researchers and healthcare professionals to better explore, understand and help ameliorate financial distress that patients may experience as a consequence of their cancer and treatments. The current review highlights a paucity of work regarding PROs used to quantify the impacts on patients’ everyday roles and responsibilities in life as a result of cancer and its treatments. Only three studies [55–57] were found, each exploring the impact on the parental role with validated tools. However, data are predominantly from female participants (see Table 1) which should be addressed with future work. The impact on any role/responsibility a patient might have towards other dependants such as elderly parents or an incapacitated spouse/partner was covered with only a single generic item on the SDI, ‘Have you had difficulty with looking after those who depend on you? (e.g. children, dependent adults, pets)’. Yet, evidence suggests that these aspects need to be included in our evaluations; exploratory qualitative analysis has shown that older women with breast cancer who cared for others struggled to balance caregiving responsibilities and their own health needs [36]. In another study, women with early-stage breast cancer and multiple caregiving roles were found to have elevated depressed mood over time [39].

Additionally, there is a survey literature [26–33], not reviewed here, documenting return to work rates and the assessment of work-related functional abilities measured using instruments such as the ‘Work Ability Index’ [79] or the ‘Work Limitations Questionnaire’ [80] in patients with, or treated for, cancer. A few qualitative studies [34, 35, 40] have described the value and meaning of paid work in patients’ lives and barriers to re-joining the workforce. However, the current review found little of patients’ own perceptions of the impact of cancer and its treatments on these aspects of life measured using a comprehensive PRO. The two validated multidimensional instruments identified (IIRS, SDI) have single items asking about impact on work amounting to nothing above that already found in the frequently used, validated, HRQoL instruments (EORCT-QLQ-C30 or FACT-G).

Two validated multidimensional PROs were identified, the IIRS [74] and SDI [10], which capture a broad range of aspects of patients’ everyday lives albeit balanced with brevity. The SDI is of particular relevance since it has been specifically developed for the oncology setting with the aim of being used as a tool to facilitate the integration of the assessment of social well-being into routine care in a way similar to that advocated for psychological well-being [76, 77]. Its purposes are to aid detection and characterisation of social problems and to improve communication between patients and healthcare professionals about this, leading to appropriate service responses, including if necessary onward referral and ultimately better care and enhanced well-being for patients. Other ways that it, and similar instruments, could be used include for the research and development of interventions to help patients manage social impacts like financial burden or family caregiving responsibilities, or perhaps as part of survivorship care plans, as well as for assessing any differential impacts of treatments being compared in clinical trials.

Nevertheless, clearly insufficient data are being gathered with patients to comprehensively understand their problems and needs to enable supporting them living well with their disease, including making decisions about ongoing treatment options. Impacts on the social domain need to be consistently assessed more comprehensively and this has implications for the current HRQoL instruments commonly used. Options for the future include using the SDI in tandem with the existing well-validated quality of life measures and/or generating further assessment modules (i.e. subscales) for the existing instruments.

Limitations

This review was intentionally restricted to identifying studies that reported the use of PRO instruments dedicated solely to the assessment of the financial situation, lifestyle, occupational circumstances, and roles and responsibilities with dependents (looking after young offspring or elderly parents) of adult cancer patients living with advanced disease. In taking this approach, we acknowledge that we have not conducted a mapping and review process of existing social domain subscales of either the general or the more specific health-related quality of life instruments available to use in oncology and that such an undertaking could reveal further useful validated measurement items. One such tool absent from the current review is the Patient-Reported Outcomes Measurement Information System (PROMIS) [81], a product of the National Institutes of Health (NIH) in the USA. This is because existing literature on its social health domain measure (which covers companionship, social isolation, social roles and activities and social support) [82] is about its development and psychometrics, meaning it either did not meet the search terms and/or inclusion criteria or did meet an exclusion criterion. However, it is likely to have significant presence in the future, and an awareness of it is important. It has an item bank approach to its method of development, has been evolved with patients and content experts and has undergone rigorous testing and validation continues to be ongoing. It has a scoring system to norm responses to the general US population with free access and use.

Conclusions

There is a need and opportunity for further work, both in terms of instrument use and development, to ensure that the social areas of patients’ lives are comprehensively assessed. Our tools must keep pace with changes happening in cancer treatment outcomes so that salient social problems are anticipated and/or ameliorated. The COST and SDI, two well-developed and validated tools, could be used to supplement shortfalls in the commonly employed HRQoL instruments. But, there is also scope for developing additional subscales within the existing modular systems to enhance them. In particular, attention needs to be directed towards roles and responsibilities, including work and patients with dependents.